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First Record of a Male of Kryptolebias Hermaphroditus Costa, 2011 (Cyprinodontiformes: Cynolebiidae)

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First Record of a Male of Kryptolebias Hermaphroditus Costa, 2011 (Cyprinodontiformes: Cynolebiidae) Neotropical Ichthyology, 14(3): e160024, 2016 Journal homepage: www.scielo.br/ni DOI: 10.1590/1982-0224-20160024 Published online: 30 September 2016 (ISSN 1982-0224) First record of a male of Kryptolebias hermaphroditus Costa, 2011 (Cyprinodontiformes: Cynolebiidae) Waldir M. Berbel-Filho1,2, Helder M. V. Espírito-Santo3 and Sergio M. Q. Lima1 During an ichthyological survey in September 2015 at the Ceará-Mirim River estuary, Rio Grande do Norte State, northeastern Brazil, we collected a male of Kryptolebias hermaphroditus, a cynolebiid species that had been previously described as containing exclusively self-fertilizing hermaphrodites. This is the first record of a male in this species, over 140 years after the discovery of the mangrove rivulid species from Brazil. Our discovery reinforces the need for more studies in K. hermaphroditus, as well as the potential of this species as a model for evolutionary studies due to its unique mating system. Durante uma amostragem ictiológica em setembro de 2015 no estuário do rio Ceará-Mirim, Estado do Rio Grande do Norte, Nordeste do Brasil, nós coletamos um macho de Kryptolebias hermaphroditus, uma espécie de rivulídeo que foi descrita como contendo apenas hermafroditas auto-fertilizantes. Este é o primeiro registro de um macho dessa espécie, mais de 140 anos depois da descoberta das espécies de rivulídeos de manguezais do Brasil. Nossa descoberta reforça a necessidade de mais estudos em K. hermaphroditus, assim como, o potencial desta espécie como um modelo para estudos evolutivos devido ao seu sistema reprodutivo único. Keywords: Hermaphroditism, Mangrove killifish, Mid-Northeastern Caatinga ecoregion, Mixed-mating system, Sexual dimorphism. Introduction 2009; Costa et al., 2010). Because of its reproductive mixed- mated system, K. marmoratus has been a popular model Although the overall taxonomy of Kryptolebias Costa, species for embryological, physiological, behavioral and 2004 is confusing (Costa, 2006), the K. marmoratus species genetic studies (Avise & Tatarenkov, 2015). While males group is well supported by both molecular (Tartarenkov et are rare in K. marmoratus, they are considered to be absent al., 2009) and morphological data (Costa et al., 2010). The in K. hermaphroditus (Costa, 2011; Tatarenkov et al., 2011), species comprising this group, K. marmoratus (Poey, 1880), despite this species having been known at least since 1868 K. ocellatus (Hensel, 1868) and K. hermaphroditus Costa, (previously known as K. ocellatus) and numerous museum 2011, inhabit estuarine areas associated with mangroves, and unpreserved specimens have been examined (Costa, ranging from southeastern United States of America to 2011). Due to the absence of males in fish collections, and southern Brazil (Costa, 2011). Besides this unusual brackish following a re-examination of the holotype of K. ocellatus, habitat, these species are also unique among aplocheiloid the monomorphic hermaphrodite species from Brazil was killifishes due to the absence of females, which are replaced described as K. hermaphroditus (Costa, 2011). by hermaphrodites (Costa et al., 2010). Hermaphrodites of both species (K. marmoratus and Indeed, self-fertilizing hermaphroditism is the dominant K. hermaphroditus) typically have a black ocellus on the mode of reproduction in Kryptolebias marmoratus caudal peduncle and a dark-grey body side (Soto & Noakes, distributed from Florida to Venezuela (Tatarenkov et al., 1994; Costa, 2011). In K. marmoratus, males exhibit a bright 2011) and K. hermaphroditus occurring in the Atlantic orange coloration on the body flank and fins, an absent or Forest mangroves of Brazil (Lira et al., 2015). This poorly-defined ocellus on the caudal peduncle, and black clade represents the only occurrence of self-fertilizing margins on the caudal fins (Davis et al., 1990; Soto & hermaphroditism among vertebrates (Tartarenkov et al., Noakes, 1994; Costa, 2011). 1Laboratório de Ictiologia Sistemática e Evolutiva, Departamento de Botânica e Zoologia, Universidade Federal do Rio Grande do Norte, Av. Senador Salgado Filho 3000, 56078-970 Natal, RN, Brazil. (SMQL) [email protected], (WMBF) [email protected] (corresponding author) 2Department of BioSciences, College of Science, Swansea University, SA2 8PP, Swansea, Wales, United Kingdom 3Post-Doctoral Program, Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo, 2936, Petrópolis, 69067-375 Manaus, AM, Brazil. [email protected] 1 Neotropical Ichthyology, 14(3): e160024, 2016 2 A male Kryptolebias hermaphroditus In a recent collection in the Ceará-Mirim River estuary, Results we found a Kryptolebias hermaphroditus individual with a male phenotype. Considering that this species has been All specimens were identified as Kryptolebias described as being completely composed of hermaphrodites, hermaphroditus on the basis of having 1-4 teeth in the the main objective of the present study is to record and vomer and a color pattern with silvery or pale golden describe the first occurrence of a male K. hermaphroditus. spots on the dorsal part of the flank. The male individual had bright orange coloration on the body flank and fins Material and Methods (mainly dorsal, anal and caudal), and black margins on the anal and caudal fins (Fig. 1), as in males of K. In September 2015, during a nocturnal exploratory marmoratus. fieldwork being conducted with the objective of designing Comparing male and hermaphroditic phenotypes an ecological study on Kryptolebias hermaphroditus at the of the captured specimens, both have a dark ocellus on Ceará-Mirim River estuary (05°40’25.9”S 35°14’14.5”W, the caudal peduncle; however, the ocellus is faint on the see Lira et al., 2015 for a map and detailed description of the male specimen. The hermaphrodites consistently exhibit area), we observed a bright orange individual of Kryptolebias a brown or grey flank coloration, as well as hyaline (Fig. 1). This specimen together with specimens exhibiting unpaired fins with pale grey dots on the basal portion, a more typical hermaphroditic appearance, were captured whereas the male individual exhibits unpaired fins with by hand and with the help of a hand sieve (50 x 60 cm, 1 orange coloration (Fig. 2). mm mesh), under permit #30532-1/2011 issued by ICMBio/ SISBIO. The fishes were euthanized using clove oil, Description. Morphometric data of male (30.1 mm SL) fixed in formalin solution, transferred to an 70% alcohol in Table 1. Urogenital papilla cylindrical in male, pocket- solution and then deposited in the ichthyological collection like shape in hermaphrodites (Fig. 3). Dorsal fin rounded. of Universidade Federal do Rio Grande do Norte (UFRN Anal fin sub-trapezoidal, distal margin slightly damaged; 3774, 8 ex.). Some other individuals, as well as a small anal-fin rays 4 and 5 longer than other anal-fin rays. Caudal fin-clip (TIUFRN 3481; tissue collection of UFRN), were fin oval, deeper than long. Pectoral fin short and rounded. directly stored in 96% ethanol for molecular analysis. Pelvic fin elliptical. Pelvic-fin bases medially separated by Measurements and counts for the orange individual short interspace. Dorsal-fin origin at vertical between 9th follow Costa (1995). Kryptolebias species identification and 10th anal-fin rays. Dorsal-fin rays 8; anal-fin rays 11; was carried out using the key proposed by Costa (2009), and caudal-fin rays 30; pectoral-fin rays 13; pelvic-fin rays 6. later confirmed using Costa (2011). To identify male traits, Scales small, cycloid. Frontal squamation E-patterned. we used the information described for the closely related Longitudinal series of scales 47; transverse series of scales species K. marmoratus (Davis et al., 1990; Soto & Noakes, 13; scale rows around caudal peduncle 25. Contact organs 1994; Costa, 2011). absent. Fig. 1. Kryptolebias hermaphroditus, male, UFRN 3774, 30.1 mm SL (three days after sampling); Ceará-Mirim River estuary, Extremoz, Rio Grande do Norte, Brazil. Neotropical Ichthyology, 14(3): e160024, 2016 W. M. Berbel-Filho, H. M. V. Espírito-Santo & S. M. Q. Lima 3 Fig. 2. Kryptolebias hermaphroditus, male (below) 30.1 mm SL, hermaphrodite (above) 35.5 mm SL, UFRN 3774, Ceará- Mirim River estuary, Extremoz, Rio Grande do Norte, Brazil. Table 1. Morphometric data of the Kryptolebias hermaphroditus, male (UFRN 3774). Standard length (mm) 30.16 Percents of standard length Body depth 17.11 Caudal-peduncle depth 13.23 Predorsal length 73.18 Prepelvic length 62.10 Length of dorsal-fin base 12.33 Length of anal-fin base 15.78 Caudal-fin length 25.86 Pectoral-fin length 17.90 Pelvic-fin length 6.63 Head length 25.10 Percents of head length Head depth 59.31 Head width 71.07 Fig. 3. Urogenital papillae of Kryptolebias hermaphroditus Snout length 29.33 in ventral view; UFRN 3374: a, cylindrical shape in male, Lower-jaw length 23.51 30.1 mm SL; b, pocket shape in hermaphrodite, 35.5 mm Eye diameter 26.55 SL. Scale bars = 1 mm. Neotropical Ichthyology, 14(3): e160024, 2016 4 A male Kryptolebias hermaphroditus Coloration. Flank dark grey on anterior and dorsal specimens with light grey and dark orange spots on the portion of head, from greyish to orange on posterior and flanks, grey humeral and caudal peduncle spots and dark ventral portions. Side of the body intensely pigmented grey to black distal zones of unpaired fins. However, this with faint dark grey stripe between postorbital region author recognized that this material was not preserved and caudal-fin base, and small irregular somewhat for study in any scientific collection and needed posterior zigzag pattern composed of small orange spots more confirmation. Posteriorly, Costa (2011) described K. concentrated on anterior half of body side. Inconspicuous hermaphroditus as only composed by hermaphrodites, dark grey humeral blotch; rounded dark spot with faint discarding the relevance of the two previous unconfirmed yellowish grey margin on dorsal end of caudal peduncle. reports. In both cases male phenotypes were reported for Rio Side of head light brown on dorsal portion, pale golden de Janeiro, where K. ocellatus (males and hermaphrodites, with dark grey dots ventrally. Jaws grey. Iris brown, with previously known as K.
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